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\begin{document}

\title{Prognostic Value of Red Blood Cell Distribution Width and D-Dimer in
Diffuse Large B-cell Lymphoma: Systematic Review and Meta-analysis.}



\author[1]{Maryam  Rahchamani }%
\author[2]{Mohammad  Sedghi }%
\author[3]{Ali  Hakimi }%
\author[4]{Mahdi  Nejatianfar }%
\author[5]{Tohid  Javaheri }%
\author[6]{Reza  Tavakoli }%
\author[5]{Ramtin  Ahmadi }%
\author[7]{Nazanin  Azmi-Naei }%
\author[3]{Neda  Kamandi }%
\author[3]{AmirMohammad  Soleimanian}%
\author[8]{Mansoureh  Makarem }%
\author[8]{Saeid  Zahmatkesh Sangani }%
\author[9]{Rasoul  Shavaleh }%
\author[9]{Kazem Rahmani}%
\author[10]{Moloud Foogerdi}%
\affil[1]{Tehran University of Medical Sciences}%
\affil[2]{Islamic Azad University}%
\affil[3]{Mashhad University of Medical Sciences}%
\affil[4]{Ferdowsi University of Mashhad}%
\affil[5]{Islamic Azad University Mashhad Branch}%
\affil[6]{Arak University of Medical Sciences}%
\affil[7]{Shahroud University of Medical Sciences}%
\affil[8]{Torbat-e Jam Faculty of Medical Sciences and Health}%
\affil[9]{Iran University of Medical Sciences}%
\affil[10]{Birjand University of Medical Sciences}%


\vspace{-1em}



  
  \date{May 24, 2024}


\begingroup
\let\center\flushleft
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\selectlanguage{english}
\begin{abstract}
Background: The significant role of red blood cell distribution width
(RDW) and D-Dimer as prognostic factors in patients with some blood
malignancies has been reported recently. Aim: We designed and performed
a meta-analysis to investigate the prognostic roles of RDW and D-Dimer
in subjects with diffuse large B-cell lymphoma (DLBCL). Materials and
Methods: We systematically reviewed PubMed-Medline, SCOPUS, EMBASE, Web
of Science Core Collection, and Google Scholar up to 30 April 2023 to
look for publications on prognostic effects of RDW and D-Dimer in DLBCL
patients. For investigation of the associations between RDW and D-Dimer
with the overall survival (OS) and progression-free survival (PFS) of
the DLBCL cases, hazard ratio (HR) with 95\% confidence intervals (CIs)
was used. Results: We included 13 eligible studies in the present
meta-analysis. The results of pooled analysis showed that increased
levels of RDW was related to poor OS (HR=2.01, 95\% CI: 1.62-2.48, P
value\textless{}0.01) and poor PFS (HR=1.52, 95\% CI: 1.24-1.85, P
value\textless{}0.01) among the DLBCL patients. On the other hand, a
significant relationship was found between increased D-Dimer and poor OS
(HR=2.30, 95\% CI: 1.03-5.14, P value\textless{}0.05) of the DLBCL
patients as well. Conclusion: Our finding clearly confirmed that
elevated RDW levels and D-Dimer were associated with adverse OS and PFS
in DLBCL.%
\end{abstract}%



\sloppy


\textbf{Introduction}

Among common types of non-Hodgkin's lymphoma, diffuse large B-cell
lymphoma (DLBCL) accounts for approximately 35\% of lymphoma cases in
western countries (1-3). Most often, chemoimmunotherapy with standard
regimens such as R-CHOP (rituximab, cyclophosphamide, doxorubicin,
vincristine prednisone) is the treatment for DLBCL patients. However,
prognosis of these patients is highly heterogeneous and it is very
difficult to predict the final outcome of the disease in the patients.
In addition, about 40\% of DLBCL patients experience relapse or are
resistant to treatment (4, 5).

In the recent years, several prognostic factors such as Hemoglobin,
Lymphocyte/Monocyte Ratio, Beta-2 microglobulin, and
Neutrophil/Lymphocyte Ratio have been proposed to project the survival
rate of DLBCL patients (6-9). Nevertheless, easier and more available
factors with high sensitivity are required for prediction of prognosis
of DLBCL patients. Red blood cell distribution width (RDW) is considered
a systemic inflammatory response marker that can be easily evaluated
through the Complete Blood Count (CBC) test and has acceptable
sensitivity in many diseases such as cardiovascular and autoimmune
diseases and sepsis (10-13). D-Dimer as a sensitive index of the process
of fibrin formation and destruction is widely used in the deep venous
thrombosis detection, intravascular coagulation, sickle cell anemia, and
myocardial infarction (14-18). Recent studies introduced that
tumor-related degradation products for the coagulation and fibrinolytic
system, such as D-Dimer, can be used as outcomes prediction for tumor
(19). Furthermore, scientific evidence recently revealed the association
of RDW and D-Dimer with many cancers such as breast cancer (20-22), lung
cancer (23, 24), blood cancers (25-27), prostate cancer (28), and other
malignancies (29-32). However, the prognostic roles of RDW and D-Dimer
in cancer and its possible mechanism in tumor progression are being
discussed. Besides, several studies indicated that D-Dimer had a
possible role in proliferation of cancer cells, adhesion, and
angiogenesis, which may bring about malignant tumors growth. Cancer
patients usually face hypercoagulable states that increase the risk of
embolism. Hence, D-Dimer levels have prognostic role and are associated
with survival of patients with cancer. Considering the differences
between the results of the studies regarding sample sizes, study
designs, and the controversy among the results, we deemed it necessary
to conduct a meta-analysis regarding comprehensively investigating the
RDW and D-Dimer prognostic roles among patients with DLBCL.

\textbf{Materials and Methods}

We utilized the Checklist of Meta-analysis of Observational Studies (33)
and preferred reporting items for systematic reviews and meta-analyses
(PRISMA) standard (34) to perform this study. The protocol was
registered with the number of CRD42023417907 at the international
prospective register of systematic reviews database (PROSPERO).

\textbf{Search Strategy}

A systematic search in PubMed, Medline, SCOPUS, Web of Science Core
Collection, EMBASE, and Google Scholar databases was carried out to find
the records from inception to 30 April 2023. Using the keywords
including RDW, red blood cell distribution width, DLBCL, diffuse large
B-cell lymphoma, lymphoma diffuse, large B-cell, fibrin fragment D,
D-dimer, D-dimer fibrin, and D-dimer fragments, two researchers (KR and
RS) searched in the mentioned databases separately and blindly.
Inconsistencies in some articles were also solved by other researchers
(NAN, MR, MF and NK). Finally, duplicates were identified by title of
the papers, authors' names, and journals' names.

\textbf{Eligibility Criteria}

We included all the observational studies which examined the role of RDW
and D-dimer as prognostic factors in DLBCL cases and also published in
English without time and place restriction. On the other hand, studies
such as case reports, case series, letters, and correspondence studies
were among our exclusion criteria (Flowchart 1). The articles conducted
regarding autoimmune diseases, Immunosuppression, patients with mental
disorders, and those undergoing dialysis were excluded as well. In
addition, the studies with lack of sufficient information on overall
survival (OS) as well as progression-free-survival (PFS) of DLBCL
subjects were excluded from the review process.

\textbf{Data Extraction and Quality Assessment}

Articles were screened independently by two researchers (RT and RM)
(according to Flowchart 1) and disagreements resolved through
discussions with other researchers. The extracted information included
author's first name, study location, study type, type of marker
investigated, year of publication, type of survival analysis performed,
mean follow-up period, sample size, and a summary of the cut-off points
for the markers investigated. OS is usually the time length from the
beginning of medical treatment until outcome occurrence (death whether
or end of the follow-up period of the patient). PFS is the duration when
the treatment is started until tumor progresses or death happens for any
reason. In order to evaluate quality of the articles, two researchers
(MR and AH) independently used the checklist of Newcastle Ottawa Scale
(NOS) (35). The articles with a total score of [?]7 were considered as
high-quality.

\textbf{Statistical Analysis}

We used R version 4.3.0 for performing the statistical analysis.
I\textsuperscript{2} and \selectlanguage{greek}χ\selectlanguage{english}\textsuperscript{2} statistics were applied
for assessing the heterogeneity of the studies and the significance
level for heterogeneity between the studies was considered
I\textsuperscript{2} \textgreater{} 50\% and P value \textless{}0.1. We
used a random effect model so as to compute Pooled Hazard Ratio with
95\% confidence interval and the Inverse Variance method was applied to
weight the studies. The researchers also used funnel plot and Eggers'
test to check the publication bias in the studies and the asymmetric
funnel plot was considered as a possible publication bias. Sensitivity
analysis was utilized to examine the heterogeneity source between the
records. The significance level in this study was considered \textless{}
0.05.

\textbf{Figure 1.} PRISMA flow diagram illustrating the process of
selection studies in the meta-analysis

\textbf{Results}

A total of 13 studies (1, 6, 7, 16, 19, 36-43) were included in our
study (PRISMA flow diagram) based on the searched databases. Overall,
eight studies (1, 6, 7, 37, 39-41, 43) focused on the role of RDW and
the remaining five studies (16, 19, 36, 38, 42) focused on D-Dimer
levels in DLBCL patients. The included studies were published from 2015
to 2022. All included articles were retrospective cohorts. Eight studies
were conducted in China (7, 16, 19, 36, 38-40, 43) and others were
conducted in Croatia (41), Iraq (37), Japan (42), Peru (1), and Spain
(6). The total sample size of the meta-analysis was 3972 people (1252
and 2720 patients in the studies were related to prognostic roles of
D-Dimer and RDW in DLBCL patients, respectively) varying from 81 to 992
people in the included studies. Other details of the included studies
are shown briefly in Table 1.

\textbf{Overall Survival in RDW and D-Dimer}

To examine the relationship between the RDW in DLBCL patients and OS,
seven studies (1, 7, 37, 39-41, 43) with 1728 patients were included.
Our findings showed that RDW levels had relationship with OS. The pooled
analysis presented a significant association between increased RDW and
adverse OS of the patients (HR \textsubscript{Pooled}= 2.01, 95\% CI:
1.62-2.48, P value\textless{}0.01) (Table 1) (Plot 2). Examining the
correlation between the D-Dimer and OS among the patients with DLBCL was
performed by four studies (16, 19, 38, 42) with 1066 patients and
D-Dimer levels correlated with poorer OS. The combined results also
demonstrated that increased D-Dimer was associated with worse OS of the
patients (HR \textsubscript{Pooled}= 2.30, 95\% CI: 1.03-5.14, P
value\textless{}0.05) (Plot 3).

\textbf{Progression-Free-Survival and RDW}

Five studies (6, 7, 37, 39, 43) with 2169 patients reported the
relationship between the RDW levels and PFS. In this study, the pooled
HRs showed that increased RDW correlated with worse PFS in the DLBCL
patients (HR \textsubscript{Pooled}=1.52, 95\% CI: 1.24-1.85, P
value\textless{}0.01) (Plot 4).

\textbf{Sensitivity Analysis}

With respect to the sensitivity analysis, the results did not show
significant difference between the included articles regarding the
relationship between RDW and D-Dimer and OS, and the relationship
between RDW and PFS among the DLBCL patients (supplementary file Figs 1,
2 and 3).

\textbf{Publication Bias}

The Funnel Plot and Eggers' test were used so as to evaluate publication
bias of the studies. We found no significant bias in the articles
included in this study (Eggers' test P value \textgreater{} 0.05). (Figs
5, 6 and 7).

\textbf{Table1-} Summary of studies on the prognostic factors such as
RDW and D-Dimer among patients with DLBCL\selectlanguage{english}
\begin{longtable}[]{@{}lllllllll@{}}
\toprule
\textbf{First Author} & \textbf{Type of Study} & \textbf{Country} &
\textbf{Year} & \textbf{Type of Marker} & \textbf{Description} &
\textbf{Type of Analysis} & \textbf{Follow up Time (Month)} &
\textbf{Sample Size}\tabularnewline
\midrule
\endhead
Atsushi Tanaka (42) & Retrospective & Japan & 2018 & D-Dimer & Cut-off
value of D-dimer \textless{} 1.0 \selectlanguage{greek}μ\selectlanguage{english}g/ml for LD and [?]1 \selectlanguage{greek}μ\selectlanguage{english}g/ml for HD & OS &
30.2 (0.1-162) & 391\tabularnewline
Yu-di GENG (19) & Retrospective & China & 2019 & D-Dimer & Cut-off value
of D-dimer 0.92 & OS & 14 (1-82) & 113\tabularnewline
Shaobo Duan (36) & Retrospective & China & 2022 & D-Dimer & - & PFS & -
& 186\tabularnewline
Bin Liu (16) & Retrospective & China & 2018 & D-Dimer & Cut-off value of
D-dimer [?]1.6 \selectlanguage{greek}μ\selectlanguage{english}g/ml & OS & 33 (1-86) & 254\tabularnewline
Haobo Huang (38) & Retrospective & China & 2021 & D-Dimer & Cut-off
value of D-dimer [?]1.4 \selectlanguage{greek}μ\selectlanguage{english}g/ml For HD and D-Dimer \textless{} 1.4 for LD &
OS, PFS & 22.13 (2.73-89.07) & 308\tabularnewline
Brady E. Beltran (1) & Retrospective & Peru & 2019 & RDW & High RDW
(\textgreater{} 14.6\%) and normal RDW (11.6\%-14.6\%). & OS & 67.2 &
121\tabularnewline
Leyre Bento (6) & Retrospective & Spain & 2019 & RDW & RDW
ratio\textgreater{}0.96 according to the new prognosis score & OS, PFS &
55 (12-185) & 992\tabularnewline
Kawa Muhamedamin Hasan (37) & Retrospective & Iraq & 2021 & RDW & High
RDW ([?] 14.85\%) and Low RDW (\textless{}14.85\%). & OS, PFS & 35 (3-133)
& 136\tabularnewline
Vlatka Peri\selectlanguage{polish}š\selectlanguage{english}a (41) & Retrospective & Croatia & 2015 & RDW & Elevated RDW
\textgreater{}15\%, Normal RDW[?]15\% & OS, ESF & 22 (8.5-37.5) &
81\tabularnewline
Danhui Li (39) & Retrospective & China & 2022 & RDW & High RDW ([?]
13.40\%), Low RDW ([?]12.60\%) and Medium RDW (13.4\% \textgreater{} RDW
\textgreater{} 12.6\%) & OS, PFS & 35 (1-82) & 179\tabularnewline
Shujuan Zhou (43) & Retrospective & China & 2017 & RDW & High RDW ([?]
14.1\%) and Low RDW (\textless{}14.1\%) & OS, PFS & 42 (6-120) &
161\tabularnewline
Manman Li (40) & Retrospective & China & 2019 & RDW & High RDW
(\textgreater{} 14.35\%) and Low RDW ([?]14.35\%) & OS, PFS & 21.3
(0.80-126.93) & 349\tabularnewline
Haizhu Chen (7) & Retrospective & China & 2022 & RDW & High RDW ([?]
14.50\%) and Low RDW (\textless{}14.50\%) & OS, PFS & 85.2 (0.5-179.6) &
701\tabularnewline
\bottomrule
\end{longtable}

\textbf{LD} ; Low D-Dimer, \textbf{HD} ; High D-Dimer, \textbf{OS} ;
Overall Survival, \textbf{PFS} ; Progression Free Survival, \textbf{EFS}
; Event Free Survival, \textbf{NOS} ; Newcastle--Ottawa Quality
Assessment Scale.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}

\textbf{Fig 2-} Forest plots of studies evaluating the relationship
between RDW and OS\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image2/image2}

\end{center}
\end{figure}

\textbf{Fig 3-} Forest plots of studies evaluating the relationship
between D-Dimer and OS\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image3/image3}

\end{center}
\end{figure}

\textbf{Fig 4-} Forest plots of studies evaluating the relationship
between RDW and PFS\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image4/image4}

\end{center}
\end{figure}

\textbf{Fig 5} - Funnel Plot with pseudo 95\% Confidence Limits for RDW
and OS\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image5/image5}

\end{center}
\end{figure}

\textbf{Fig 6} - Funnel Plot with pseudo 95\% Confidence Limits for RDW
and PFS\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image6/image6}

\end{center}
\end{figure}

\textbf{Fig 7} - Funnel Plot with pseudo 95\% Confidence Limits for
D-Dimer and OS

\textbf{Discussion}

The prognostic roles of RDW and D-Dimer were explored in subjects with
DLBCL. We observed that high RDW and D-Dimer were two prognostic factors
related to OS and PFS among DLBCL cases. Recently, evidence has been
confirmed the relationship between RDW and poor prognosis in various
cancers (44, 45). Furthermore, increased RDW was associated with worse
prognosis in blood malignancies such as chronic myeloid leukemia (46),
chronic lymphocytic leukemia (47), NK/T lymphoma (48), multiple myeloma
(49), and DLBCL (40).

Inflammation is a pivotal factor which plays a role in progression of
tumor and is known as one of its prominent features (25, 50). In this
study, the pooled analysis results revealed that high values of RDW were
associated with poor PFS and OS. Although the main mechanism of the
relationship between RDW and the prognosis of DLBCL patients has not
been clearly and fully investigated, high RDW can be attributed to the
disturbance in erythropoiesis and the changes in red blood cell
maturation (51).

Some findings have provided evidence that there is an association
between RDW and some markers such as IL-6, CRP (C - reactive protein),
TNF-I and II (Tumor Necrosis Factor), TK (Thymidine Kinase), ESR
(Erythrocyte Sedimentation Rate), and Ferritin which the accuracy and
sensitivity in DLBCL patients are in a state of ambiguity (13). The
relationship between RDW and malnutrition conditions might be explained
by treatment with poor response and poor prognosis of patients who
suffer from cancer (41). In addition, the disruption in iron absorption
and metabolism mechanism observed in most cancers also contributes to
increase the level of RDW (52), and increased RDW is considered as a
turning point in the relationship between inflammation and worse
prognosis of subjects who suffer from DLBCL. On the other hand, poor
coagulation conditions are associated with poor prognosis and the
outcomes such as VTE (venous thrombosis embolism) and DIC (disseminated
intravascular coagulation).

Treatment of various cancers is associated with hypercoagulable states
and according to the evidence, the changes in coagulation and
fibrinolysis pathways have a great impact on cancer prognosis
(19).Moreover, tumor-related degradation products such as D-Dimer as a
prognostic factor of the final outcome should be used in all types of
cancer (20, 26, 29). Some studies have indicated that elevated D-Dimer
values as a suitable factor in solid tumor patients is associated with
poor prognosis (53) and D-Dimer decreases significantly after the first
chemotherapy (19). Also, it has been proved that there is an association
between values of D-Dimer and tumor progression, distant metastasis, and
tumor volume (54, 55). However, our pooled analysis results showed that
by increasing in the D-Dimer values as a prognostic factor, we witnessed
worsening OS in the DLBCL patients.

In this study, our findings determined the prognostic role of RDW and
D-Dimer in DLBCL patients. Since the values of RDW and D-Dimer can be
easily accessible in the patient tests at low cost, considering to these
prognostic indicators would be helpful in the prognosis of DLBCL
patients. However, the present study had some limitations. As a result
of small number of publications on the role of D-Dimer in DLBCL
patients, it was not possible to provide PFS in this study. On the other
hand, the basic values for grouping the individuals based on RDW were
different in the studies. Therefore, we could not be able to conduct
subgroup analysis.

\textbf{Conclusion}

This meta-analysis indicated that high values of RDW and D-Dimer were
significantly associated with low prognosis and poor OS and PFS in DLBCL
patients. Due to availability in routine laboratory tests and
affordability, they could be helpful in disease progression and
prognosis of DLBCL patients and also in clinical decisions.
Nevertheless, doing further studies in this field seems necessary.

\textbf{Author contribution:}

KR, RSH, MN and MF designed and implemented the study, performed
analysis, interpreted the data, and contributed to drafting the
manuscript. MR and AH assessed quality of studies. KR, NK, AMS and MS
interpreted the data, drafted and revised the manuscript. RT and RM
extracted the data and contributed to the data management. All authors
read and approved the submitted manuscript.

\textbf{Acknowledgment:}

Not applicable.

\textbf{Funding:}

Not applicable.

\textbf{Conflict of interest statement:}

Not applicable.

\textbf{Data availability:}

The original contributions presented in the study are included in the
article/Supplementary material, further inquiries can be directed to the
corresponding author.

\textbf{Ethnical approval statement:}

Not applicable.

\textbf{Patient consent statement:}

Not applicable.

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